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Aliivibrio fischeri

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Aliivibrio fischeri
Aliivibrio fischeri glowing on a petri dish
Scientific classification Edit this classification
Domain: Bacteria
Phylum: Pseudomonadota
Class: Gammaproteobacteria
Order: Vibrionales
Family: Vibrionaceae
Genus: Aliivibrio
Species:
A. fischeri
Binomial name
Aliivibrio fischeri
(Beijerinck 1889) Urbanczyk et al. 2007
Synonyms[1]

Aliivibrio fischeri (formerly Vibrio fischeri) is a Gram-negative, rod-shaped bacterium found globally in marine environments.[2] This bacterium grows most effectively in water with a salt concentration at around 20g/L, and at temperatures between 24 and 28°C.[3] This species is non-pathogenic[3] and has bioluminescent properties. It is found predominantly in symbiosis with various marine animals, such as the Hawaiian bobtail squid. It is heterotrophic, oxidase-positive, and motile by means of a tuft of polar flagella.[4] Free-living A. fischeri cells survive on decaying organic matter. The bacterium is a key research organism for examination of microbial bioluminescence, quorum sensing, and bacterial-animal symbiosis.[5] It is named after Bernhard Fischer, a German microbiologist.[6]

Ribosomal RNA comparison led to the reclassification of this species from genus Vibrio to the newly created Aliivibrio in 2007.[7] The change is valid publication, and according to LPSN the correct name.[8] However, the name change is not generally accepted by most researchers, who still publish using the nameVibrio fischeri (see Google Scholar for 2018–2019).

Genome

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The genome for A. fischeri was completely sequenced in 2004 and consists of two chromosomes, one smaller and one larger. Chromosome 1 has 2.9 million base pairs (Mbp) and chromosome 2 has 1.3 Mbp, bringing the total genome to 4.2 Mbp.

A. fischeri has the lowest G+C content of 27 Vibrio species, but is still most closely related to the higher-pathogenicity species such as V. cholerae. The genome for A. fischeri also carries mobile genetic elements.[9] The precise functions of these elements in A. fischeri are not fully understood. However, they are known to play a role in acquiring genes associated with virulence and resistance to environmental stresses in other bacterial species.[10]

Some strains of A. fischeri, such as strain ES114, contain a plasmid. The plasmid in strain ES114 is called pES100 and is most likely used for conjugation purposes. This purpose was determined based on the 45.8 kbp gene sequence, most of which codes for a type IV section system. The ability to preform conjugation can be helpful for both beneficial and pathogenic strains, as it allows for DNA exchange.[11]

There is also evidence that the genome of A. fischeri includes pilus gene clusters. These clusters encode for many different kinds of pili, which serve a variety of functions. In this species, there are pili used for pathogenesis, twitching motility, tight adhesion, and toxin-coregulation, and more.[11]

Ecology

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The Hawaiian bobtail squid, its photophores populated with Aliivibrio fischeri

A. fischeri are globally distributed in temperate and subtropical marine environments.[12] They can be found free-floating in oceans, as well as associated with marine animals, sediment, and decaying matter.[12] A. fischeri have been most studied as symbionts of marine animals, including squids in the genus Euprymna and Sepiola, where A. fischeri can be found in the squids' light organs.[12] This relationship has been best characterized in the Hawaiian bobtail squid (Euprymna scolopes). A. fischeri is the only species of bacteria inhabiting the squid's light organ,[13] despite an environment full of other bacteria.[14]

Symbiosis with the Hawaiian bobtail squid

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A. fischeri colonization of the light organ of the Hawaiian bobtail squid is currently studied as a simple model for mutualistic symbiosis, as it contains only two species and A. fischeri can be cultured in a lab and genetically modified. Aliivibrio fischeri utilizes chitin as a primary carbon and nitrogen source in its symbiosis with the Hawaiian bobtail squid. In the squid’s light organ, A. fischeri breaks down chitin into N-acetylglucosamine (GlcNAc), which acts as both a nutrient and a chemoattractant, guiding colonization. Chitinases facilitate this breakdown, while the regulatory protein NagC controls gene expression for chitin and GlcNAc use. The bacteria metabolize GlcNAc through fermentation or respiration, supporting energy needs and bioluminescence, which are crucial for the mutualistic relationship with the squid. [15]This mutualistic symbiosis provides A. fischeri with nutrients and a protected environment and helps the squid avoid predation using bioluminescence.

A. fischeri provides luminescence by colonizing the light organ of the Hawaiian bobtail squid[16], which is on its ventral side[14]. The organ luminesces at night, providing the squid with counter-illumination camouflage. The light organs of certain squid contain reflective plates that intensify and direct the light produced, due to proteins known as reflectins. They regulate the light intensity to match that of the sea surface below.[16] This strategy prevents the squid from casting a shadow on the ocean floor, helping it avoid predation during feeding[14][16]. The A. fischeri population is maintained by daily cycles. About 90% of A. fischeri are ejected by the squid every morning in a process known as "venting".The 10% of bacteria remaining in the squid replenish the bacterial population before the following night.[14]

A. fischeri are horizontally acquired by young squids from their environment. Venting is thought to provide the source from which newly hatched squid are colonized. This colonization induces developmental and morphological changes in the squid's light organ, which is translucent [14][16]. Interestingly, certain morphological changes made by A. fischeri do not occur when the microbe cannot luminesce, indicating that bioluminescence (described below) is truly essential for symbiosis. In the process of colonization, ciliated cells within the animals' photophores (light-producing organs) selectively draw in the symbiotic bacteria. These cells create microcurrents that, when combined with mucus[17], promote the growth of the symbionts and actively reject any competitors. The bacteria cause the ciliated cells to die off once the light organ is sufficiently colonized[16].

Bioluminescence

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The bioluminescence of A. fischeri is caused by transcription of the lux operon, and the following translation of the lux proteins, which produce the light. This process is induced through population-dependent quorum sensing.[2] The population of A. fischeri needs to reach an optimal level to activate the lux operon and stimulate light production. The circadian rhythm controls light expression, where luminescence is much brighter during the day and dimmer at night, as required for camouflage.

The bacterial luciferin-luciferase system is encoded by a set of genes labelled the lux operon. In A. fischeri, five such genes (luxCDABEG) have been identified as active in the emission of visible light, and two genes (luxR and luxI) are involved in regulating the operon. Several external and intrinsic factors appear to either induce or inhibit the transcription of this gene set and produce or suppress light emission.

A. fischeri is one of many species of bacteria that commonly form symbiotic relationships with marine organisms.[18] Marine organisms contain bacteria that use bioluminescence so they can find mates, ward off predators, attract prey, or communicate with other organisms.[19] In return, the organism the bacteria are living within provides the bacteria with a nutrient-rich environment.[20] The lux operon is a 9-kilobase fragment of the A. fischeri genome that controls bioluminescence through the catalytic activity of the enzyme luciferase.[21] This operon has a known gene sequence of luxCDAB(F)E, where luxA and luxB code for the protein subunits of the luciferase enzyme, and the luxCDE codes for a fatty acid reductase complex that makes the fatty acids necessary for the luciferase mechanism.[21] luxC codes for the enzyme acyl-reductase, luxD codes for acyl-transferase, and luxE makes the proteins needed for the enzyme acyl-protein synthetase. Luciferase produces blue/green light through the oxidation of reduced flavin mononucleotide and a long-chain aldehyde by diatomic oxygen. The reaction is summarized as:[22]

FMNH2 + O2 + R-CHO → FMN + R-COOH + H2O + light.

The reduced flavin mononucleotide (FMNH) is provided by the fre gene, also referred to as luxG. In A. fischeri, it is directly next to luxE (giving luxCDABE-fre) from 1042306 to 1048745 [1]

To generate the aldehyde needed in the reaction above, three additional enzymes are needed. The fatty acids needed for the reaction are pulled from the fatty acid biosynthesis pathway by acyl-transferase. Acyl-transferase reacts with acyl-ACP to release R-COOH, a free fatty acid. R-COOH is reduced by a two-enzyme system to an aldehyde. The reaction is:[20]

R-COOH + ATP + NADPH → R-CHO + AMP + PP + NADP+.

Quorum sensing

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Quorum sensing in Aliivibrio fischeri [23]
Green pentagons denote AHL autoinducer that LuxI produces (3OC6-homoserine lactone). Transcriptional regulator, LuxR, modulates expression of AHL synthase, LuxI, and the lux operon, leading to luciferase-mediated light emission

One primary system that controls bioluminescence through regulation of the lux operon is quorum sensing, a conserved mechanism across many microbial species that regulates gene expression in response to bacterial concentration. Quorum sensing functions through the production of an autoinducer, usually a small organic molecule, by individual cells. As cell populations increase, levels of autoinducers increase, and specific proteins that regulate transcription of genes bind to these autoinducers, altering gene expression. This system allows microbial cells to "communicate" amongst each other and coordinate behaviors, such as luminescence, which require large amounts of cells to produce a noticeable effect.[23]

In A. fischeri, there are two primary quorum sensing systems, each of which responds to slightly different environments. The first system is commonly referred to as the lux system, as it is encoded within the lux operon, and uses the autoinducer 3OC6-HSL.[24] The protein LuxI synthesizes this signal, which is subsequently released from the cell. This signal, 3OC6-HSL, then binds to the protein LuxR, which regulates the expression of many different genes, but most notably upregulation of genes involved in luminescence.[25] The second system, commonly referred to as the ain system, uses the autoinducer C8-HSL, which is produced by the protein AinS. Similar to the lux system, the autoinducer C8-HSL increases activation of LuxR. In addition, C8-HSL binds to another transcriptional regulator, LitR, giving the ain and lux systems of quorum sensing slightly different genetic targets within the cell.[26]

The different genetic targets of the ain and lux systems are essential, because these two systems respond to different cellular environments. The ain system regulates transcription in response to intermediate cell density cell environments, producing lower levels of luminescence and even regulating metabolic processes such as the acetate switch.[27] In contrast, the lux quorum sensing system occurs in response to high cell densities, producing high levels of luminescence and regulating the transcription of additional genes, including QsrP, RibB, and AcfA.[28] Both of the ain and lux quorum sensing systems are essential for colonization of the squid and regulate multiple colonization factors in the bacteria.[25]

Activation of the lux operon by LuxR and LuxI in Aliivibrio fischeri [29][30]
(A) At low cell density, the autoinducers (3OC6-HSL – red dots), produced by LuxI, diffuse through the cell membrane into the growth medium
(B) As the cell growth continues, the autoinducers in the medium start to accumulate in a confined environment. A very low intensity of light can be detected.
(C) When enough autoinducers have accumulated in the medium, they can re-enter the cell where they directly bind the LuxR protein to activate luxICDABEG expression.
(D) High levels of autoinducers activate the luminescent system of A. fischeri. A high intensity of light can be detected.

Research Applications

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A. fischeri has broad applications in ecotoxicology and environmental research. Its bioluminescence is sensitive to toxicants, and reductions in light emission are used in bioassays like the Microtox test to assess water quality.[31] It also plays a key role in studying the effects of chemical mixtures, helping identify synergistic or antagonistic toxic interactions. [32] In biotechnology, its light-producing mechanism is harnessed for developing biosensors that detect environmental pollutants in real time, making it a valuable tool in pollution monitoring and water treatment studies. The bacteria’s adaptation to competitive marine environments, where it may produce unique bioactive compounds, may also position it as a useful organism for discovering novel antibiotics from marine sources. [33]

Natural transformation

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Natural bacterial transformation is an adaptation for transferring DNA from one individual cell to another. Natural transformation, including the uptake and incorporation of exogenous DNA into the recipient genome, has been demonstrated in A. fischeri.[34] This process is induced by chitohexaose and is likely regulated by genes tfoX and tfoY. Natural transformation of A. fischeri facilitates rapid transfer of mutant genes across strains and provides a valuable tool for experimental genetic manipulation in this species.

State microbe status

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In 2014, Hawaiʻian State Senator Glenn Wakai submitted SB3124 proposing Aliivibrio fischeri as the state microbe of Hawaiʻi.[35] The bill was in competition with a bill to make Flavobacterium akiainvivens the state microbe, but neither passed. In 2017, legislation similar to the original 2013 F. akiainvivens bill was submitted in the Hawaiʻi House of Representatives by Isaac Choy[36] and in the Hawaiʻi Senate by Brian Taniguchi.[37]

List of synonyms

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  • Achromobacter fischeri (Beijerinck 1889) Bergey et al. 1930
  • Bacillus fischeri (Beijerinck 1889) Trevisan 1889
  • Bacterium phosphorescens indigenus (Eisenberg 1891) Chester 1897
  • Einheimischer leuchtbacillus Fischer 1888
  • Microspira fischeri (Beijerinck 1889) Chester 1901
  • Microspira marina (Russell 1892) Migula 1900
  • Photobacterium fischeri Beijerinck 1889
  • Vibrio noctiluca Weisglass and Skreb 1963 [1]

See also

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References

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  17. ^ Nyholm SV, McFall-Ngai MJ (2021-10). "A lasting symbiosis: how the Hawaiian bobtail squid finds and keeps its bioluminescent bacterial partner". Nature Reviews Microbiology. 19 (10): 666–679. doi:10.1038/s41579-021-00567-y. ISSN 1740-1526. {{cite journal}}: Check date values in: |date= (help)
  18. ^ Girish S, Ravi L (January 2023). "Vibrio fischeri in squid light organ.". In Dharumadurai D (ed.). Microbial Symbionts. Academic Press. pp. 511–520. doi:10.1016/B978-0-323-99334-0.00006-2. ISBN 978-0-323-99334-0.
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  22. ^ Silverman et al., 1984
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  24. ^ Eberhad A (1981). "Structural identification of autoinducer of Photobacterium fischeri luciferase". Biochemistry. 20 (9): 2444–2449. doi:10.1021/bi00512a013. PMID 7236614. Retrieved 2020-04-26.
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  27. ^ Studer SV, Mandel MJ, Ruby EG (September 2008). "AinS quorum sensing regulates the Vibrio fischeri acetate switch". Journal of Bacteriology. 190 (17): 5915–5923. doi:10.1128/JB.00148-08. PMC 2519518. PMID 18487321.
  28. ^ Qin N, Callahan SM, Dunlap PV, Stevens AM (June 2007). "Analysis of LuxR regulon gene expression during quorum sensing in Vibrio fischeri". Journal of Bacteriology. 189 (11): 4127–4134. doi:10.1128/JB.01779-06. PMC 1913387. PMID 17400743.
  29. ^ Li Z, Nair SK (October 2012). "Quorum sensing: how bacteria can coordinate activity and synchronize their response to external signals?". Protein Science. 21 (10): 1403–1417. doi:10.1002/pro.2132. PMC 3526984. PMID 22825856.
  30. ^ Tanet L, Tamburini C, Baumas C, Garel M, Simon G, Casalot L (2019). "Bacterial Bioluminescence: Light Emission in Photobacterium phosphoreum Is Not Under Quorum-Sensing Control". Frontiers in Microbiology. 10: 365. doi:10.3389/fmicb.2019.00365. PMC 6409340. PMID 30886606. Material was copied from this source, which is available under a Creative Commons Attribution 4.0 International License
  31. ^ Backhaus T, Froehner K, Altenburger R, Grimme LH (1997-12-01). "Toxicity testing with Vibrio Fischeri: A comparison between the long term (24 h) and the short term (30 min) bioassay". Chemosphere. 35 (12): 2925–2938. Bibcode:1997Chmsp..35.2925B. doi:10.1016/S0045-6535(97)00340-8. ISSN 0045-6535.
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  35. ^ Cave J (3 April 2014). "Hawaii, Other States Calling Dibs On Official State Bacteria". Huffington Post. Retrieved 24 October 2017.
  36. ^ Choy I (25 January 2017). "HB1217". Hawaii State Legislature. Honolulu, HI: Hawaii State Legislature. Retrieved 22 October 2017.
  37. ^ Taniguchi B (25 January 2017). "SB1212". Hawaii State Legislature. Honolulu, HI: Hawaii State Legislature. Retrieved 22 October 2017.
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